JAK/STAT Signaling Regulated Intestinal Regeneration Defends Insect Pests Against Pore-forming Toxins Produced by Bacillus Thuringiensis

Overview

Journal PLoS Pathog

Specialty Microbiology

Date 2024 Jan 18

PMID 38236820

Authors

Zeyu Wang

Yanchao Yang

Sirui Li

Weihua Ma

Kui Wang

Mario Soberon

Shuo Yan

Jie Shen

Frederic Francis

Alejandra Bravo

Jie Zhang

Affiliations

Soon will be listed here.

Abstract

A variety of coordinated host-cell responses are activated as defense mechanisms against pore-forming toxins (PFTs). Bacillus thuringiensis (Bt) is a worldwide used biopesticide whose efficacy and precise application methods limits its use to replace synthetic pesticides in agricultural settings. Here, we analyzed the intestinal defense mechanisms of two lepidopteran insect pests after intoxication with sublethal dose of Bt PFTs to find out potential functional genes. We show that larval intestinal epithelium was initially damaged by the PFTs and that larval survival was observed after intestinal epithelium regeneration. Further analyses showed that the intestinal regeneration caused by Cry9A protein is regulated through c-Jun NH (2) terminal kinase (JNK) and Janus tyrosine kinase/signal transducer and activator of transcription (JAK/STAT) signaling pathways. JAK/STAT signaling regulates intestinal regeneration through proliferation and differentiation of intestinal stem cells to defend three different Bt proteins including Cry9A, Cry1F or Vip3A in both insect pests, Chilo suppressalis and Spodoptera frugiperda. Consequently, a nano-biopesticide was designed to improve pesticidal efficacy based on the combination of Stat double stranded RNA (dsRNA)-nanoparticles and Bt strain. This formulation controlled insect pests with better effect suggesting its potential use to reduce the use of synthetic pesticides in agricultural settings for pest control.

Citing Articles

JAK/STAT signaling regulated intestinal regeneration defends insect pests against pore-forming toxins produced by Bacillus thuringiensis.

Wang Z, Yang Y, Li S, Ma W, Wang K, Soberon M PLoS Pathog. 2024; 20(1):e1011823.

PMID: 38236820 PMC: 10796011. DOI: 10.1371/journal.ppat.1011823.

References

Meftaul I, Venkateswarlu K, Dharmarajan R, Annamalai P, Megharaj M . Pesticides in the urban environment: A potential threat that knocks at the door. Sci Total Environ. 2019; 711:134612. DOI: 10.1016/j.scitotenv.2019.134612. View

Brito C, Cabanes D, Mesquita F, Sousa S . Mechanisms protecting host cells against bacterial pore-forming toxins. Cell Mol Life Sci. 2018; 76(7):1319-1339. PMC: 6420883. DOI: 10.1007/s00018-018-2992-8. View

Buchon N, Broderick N, Poidevin M, Pradervand S, Lemaitre B . Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe. 2009; 5(2):200-11. DOI: 10.1016/j.chom.2009.01.003. View

Yang X, Wang Z, Geng L, Chi B, Liu R, Li H . Vip3Aa domain IV and V mutants confer higher insecticidal activity against Spodoptera frugiperda and Helicoverpa armigera. Pest Manag Sci. 2022; 78(6):2324-2331. DOI: 10.1002/ps.6858. View

Boumard B, Bardin A . An amuse-bouche of stem cell regulation: Underlying principles and mechanisms from adult Drosophila intestinal stem cells. Curr Opin Cell Biol. 2021; 73:58-68. DOI: 10.1016/j.ceb.2021.05.007. View

Nelson E, Walker S, Kepich A, Gashin L, Hideshima T, Ikeda H . Nifuroxazide inhibits survival of multiple myeloma cells by directly inhibiting STAT3. Blood. 2008; 112(13):5095-102. PMC: 2597607. DOI: 10.1182/blood-2007-12-129718. View

Li Y, Wang Z, Romeis J . Managing the Invasive Fall Armyworm through Biotech Crops: A Chinese Perspective. Trends Biotechnol. 2020; 39(2):105-107. DOI: 10.1016/j.tibtech.2020.07.001. View

Lee K, Lestradet M, Socha C, Schirmeier S, Schmitz A, Spenle C . Enterocyte Purge and Rapid Recovery Is a Resilience Reaction of the Gut Epithelium to Pore-Forming Toxin Attack. Cell Host Microbe. 2016; 20(6):716-730. DOI: 10.1016/j.chom.2016.10.010. View

Tabashnik B, Carriere Y . Surge in insect resistance to transgenic crops and prospects for sustainability. Nat Biotechnol. 2017; 35(10):926-935. DOI: 10.1038/nbt.3974. View

10.

Rodriguez-Fernandez I, Tauc H, Jasper H . Hallmarks of aging Drosophila intestinal stem cells. Mech Ageing Dev. 2020; 190:111285. DOI: 10.1016/j.mad.2020.111285. View

11.

Los F, Kao C, Smitham J, McDonald K, Ha C, Peixoto C . RAB-5- and RAB-11-dependent vesicle-trafficking pathways are required for plasma membrane repair after attack by bacterial pore-forming toxin. Cell Host Microbe. 2011; 9(2):147-57. PMC: 3057397. DOI: 10.1016/j.chom.2011.01.005. View

12.

Romero M, Keyel M, Shi G, Bhattacharjee P, Roth R, Heuser J . Intrinsic repair protects cells from pore-forming toxins by microvesicle shedding. Cell Death Differ. 2017; 24(5):798-808. PMC: 5423106. DOI: 10.1038/cdd.2017.11. View

13.

Wang Z, Yang Y, Li S, Ma W, Wang K, Soberon M . JAK/STAT signaling regulated intestinal regeneration defends insect pests against pore-forming toxins produced by Bacillus thuringiensis. PLoS Pathog. 2024; 20(1):e1011823. PMC: 10796011. DOI: 10.1371/journal.ppat.1011823. View

14.

Salem T, Allam W, Thiem S . Verifying the stability of selected genes for normalization in Q PCR experiments of Spodoptera frugiperda cells during AcMNPV infection. PLoS One. 2014; 9(10):e108516. PMC: 4196776. DOI: 10.1371/journal.pone.0108516. View

15.

Mundorf J, Donohoe C, McClure C, Southall T, Uhlirova M . Ets21c Governs Tissue Renewal, Stress Tolerance, and Aging in the Drosophila Intestine. Cell Rep. 2019; 27(10):3019-3033.e5. PMC: 6581828. DOI: 10.1016/j.celrep.2019.05.025. View

16.

Gampel A, Ring J, Virdee K, Kirov N, Tolkovsky A, Martinez-Arias A . puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 1998; 12(4):557-70. PMC: 316530. DOI: 10.1101/gad.12.4.557. View

17.

Qin F, Liu W, Wu N, Zhang L, Zhang Z, Zhou X . Invasion of midgut epithelial cells by a persistently transmitted virus is mediated by sugar transporter 6 in its insect vector. PLoS Pathog. 2018; 14(7):e1007201. PMC: 6082570. DOI: 10.1371/journal.ppat.1007201. View

18.

Buchon N, Broderick N, Chakrabarti S, Lemaitre B . Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev. 2009; 23(19):2333-44. PMC: 2758745. DOI: 10.1101/gad.1827009. View

19.

Bardin A, Perdigoto C, Southall T, Brand A, Schweisguth F . Transcriptional control of stem cell maintenance in the Drosophila intestine. Development. 2010; 137(5):705-14. PMC: 2827683. DOI: 10.1242/dev.039404. View

20.

Wang Z, Wang K, Bravo A, Soberon M, Cai J, Shu C . Coexistence of with the Gene in an Identical Plasmid of Indicates Their Synergistic Insecticidal Toxicity. J Agric Food Chem. 2020; 68(47):14081-14090. DOI: 10.1021/acs.jafc.0c05304. View